Cited by 734SARS-CoV-2 and COVID-19 ResearchT-cell and B-cell ImmunologyCOVID-19 Clinical Research Studies

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Loss of Bcl-6-Expressing T Follicular Helper Cells and Germinal Centers in COVID-19

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Kaneko, Naoki, Kuo, Hsiao-Hsuan, Boucau, Julie, Farmer, Jocelyn R., Allard-Chamard, Hugues, Mahajan, Vinay S., Piechocka-Trocha, Alicja, Lefteri, Kristina, Osborn, Matthew, Bals, Julia, Bartsch, Yannic C., Bonheur, Nathalie, Caradonna, Timothy M., Chevalier, Josh, Chowdhury, Fatema, Diefenbach, Thomas J., Einkauf, Kevin, Fallon, Jon, Feldman, Jared, Finn, Kelsey K., Garcia-Broncano, Pilar, Hartana, Ciputra Adijaya, Hauser, Blake M., Jiang, Chenyang, Kaplonek, Paulina, Karpell, Marshall, Koscher, Eric C., Lian, Xiaodong, Liu, Hang, Liu, Jinqing, Ly, Ngoc L., Michell, Ashlin R., Rassadkina, Yelizaveta, Seiger, Kyra, Sessa, Libera, Shin, Sally, Singh, Nishant, Sun, Weiwei, Sun, Xiaoming, Ticheli, Hannah J., Waring, Michael T., Zhu, Alex L., Alter, Galit, Li, Jonathan Z., Lingwood, Daniel, Schmidt, Aaron G., Lichterfeld, Mathias, Walker, Bruce D., Yu, Xu G., Padera, Robert F., Pillai, Shiv·2020·Cell

DOI 10.1016/j.cell.2020.08.025PMC PMC7437499

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Abstract

Humoral responses in coronavirus disease 2019 (COVID-19) are often of limited durability, as seen with other human coronavirus epidemics. To address the underlying etiology, we examined post mortem thoracic lymph nodes and spleens in acute SARS-CoV-2 infection and observed the absence of germinal centers and a striking reduction in Bcl-6+ germinal center B cells but preservation of AID+ B cells. Absence of germinal centers correlated with an early specific block in Bcl-6+ T FH cell differentiation together with an increase in T-bet+ T H1 cells and aberrant extra-follicular TNF-α accumulation. Parallel peripheral blood studies revealed loss of transitional and follicular B cells in severe disease and accumulation of SARS-CoV-2-specific "disease-related" B cell populations. These data identify defective Bcl-6+ T FH cell generation and dysregulated humoral immune induction early in COVID-19 disease, providing a mechanistic explanation for the limited durability of antibody responses in coronavirus infections, and suggest that achieving herd immunity through natural infection may be difficult.

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Authors: Kaneko, N., Kuo, H.-H., Boucau, J., Farmer, J. R., Allard-Chamard, H., Mahajan, V. S., Piechocka-Trocha, A., Lefteri, K., Osborn, M., Bals, J., Bartsch, Y. C., Bonheur, N., Caradonna, T. M., Chevalier, J., Chowdhury, F., Diefenbach, T. J., Einkauf, K., Fallon, J., Feldman, J., Finn, K. K., Garcia-Broncano, P., Hartana, C. A., Hauser, B. M., Jiang, C., Kaplonek, P., Karpell, M., Koscher, E. C., Lian, X., Liu, H., Liu, J., Ly, N. L., Michell, A. R., Rassadkina, Y., Seiger, K., Sessa, L., Shin, S., Singh, N., Sun, W., Sun, X., Ticheli, H. J., Waring, M. T., Zhu, A. L., Alter, G., Li, J. Z., Lingwood, D., Schmidt, A. G., Lichterfeld, M., Walker, B. D., Yu, X. G., Padera, R. F., & Pillai, S.
Affiliations: Ragon Institute of MGH, MIT and Harvard (US)
Brigham and Women's Hospital (US)
Howard Hughes Medical Institute (US)
Harvard University (US)
Corresponding author: Padera, Robert F.
Pillai, Shiv
ORCID: Kaneko, Naoki
Kuo, Hsiao-Hsuan
Boucau, Julie
Farmer, Jocelyn R.
Allard-Chamard, Hugues
Mahajan, Vinay S.
Osborn, Matthew
Bals, Julia
Bartsch, Yannic C.
Caradonna, Timothy M.
Chevalier, Josh
Chowdhury, Fatema
Diefenbach, Thomas J.
Einkauf, Kevin
Fallon, Jon
Feldman, Jared
Garcia-Broncano, Pilar
Hartana, Ciputra Adijaya
Hauser, Blake M.
Jiang, Chenyang
Lian, Xiaodong
Liu, Hang
Michell, Ashlin R.
Rassadkina, Yelizaveta
Seiger, Kyra
Sessa, Libera
Shin, Sally
Singh, Nishant
Sun, Weiwei
Sun, Xiaoming
Waring, Michael T.
Zhu, Alex L.
Alter, Galit
Li, Jonathan Z.
Lingwood, Daniel
Schmidt, Aaron G.
Lichterfeld, Mathias
Walker, Bruce D.
Yu, Xu G.
Padera, Robert F.
Pillai, Shiv
Venue: Cell
Publisher: Elsevier BV
Published: 2020-10
Volume: 183
Issue: 1
Pages: 143-157.e13
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2020.08.025
PMC: PMC7437499
OpenAlex: W3049048202
Cited by: 734
References: 51
Citations by year: 2026: 31 · 2025: 48 · 2024: 69 · 2023: 105 · 2022: 174 · 2021: 244 · 2020: 62
FWCI: 19.19
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 365 d)
Locations: Cell (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
Topics: Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
Keywords: COVID-19 pandemic, SARS-CoV-2, BCL6, T follicular helper cells, germinal center, humoral immune response, T-bet, Th1 cells, TNF-α, transitional B cells, follicular B cells, spleen, herd immunity
MeSH terms: COVID-19, Aged, Aged, 80 and over, B-Lymphocytes, Female, T-Lymphocytes, Helper-Inducer, Humans, Male, Middle Aged, Pneumonia, Viral, Spleen, Tumor Necrosis Factor-alpha, Coronavirus Infections, Germinal Center, Proto-Oncogene Proteins c-bcl-6, Pandemics

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Loss of Bcl-6-Expressing T Follicular Helper Cells and Germinal Centers in COVID-19

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